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The Relationship Between Gut Microbiota, Short-Chain Fatty Acids and Glucose Metabolism

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The Relationship Between Gut Microbiota, Short-Chain Fatty Acids and Glucose Metabolism Acta Diabetologica (2021) 58:1131–1138 https://doi.org/10.1007/s00592-021-01727-5 REVIEW ARTICLE The relationship between gut microbiota, short‑chain fatty acids and type 2 diabetes mellitus: the possible role of dietary fbre Dominic Salamone1 · Angela Albarosa Rivellese1,2 · Claudia Vetrani1,2 Received: 19 January 2021 / Accepted: 19 April 2021 / Published online: 10 May 2021 © The Author(s) 2021 Abstract Gut microbiota and its metabolites have been shown to infuence multiple physiological mechanisms related to human health. Among microbial metabolites, short-chain fatty acids (SCFA) are modulators of diferent metabolic pathways. On the other hand, several studies suggested that diet might infuence gut microbiota composition and activity thus modulating the risk of metabolic disease, i.e. obesity, insulin resistance and type 2 diabetes. Among dietary component, dietary fbre may play a pivotal role by virtue of its prebiotic efect on fbre-fermenting bacteria, that may increase SCFA production. The aim of this review was to summarize and discuss current knowledge on the impact of dietary fbre as modulator of the relationship between glucose metabolism and microbiota composition in humans. More specifcally, we analysed evidence from obser- vational studies and randomized nutritional intervention investigating the relationship between gut microbiota, short-chain fatty acids and glucose metabolism. The possible mechanisms behind this association were also discussed. Keywords Gut microbiota · Short-chain fatty acids · Type 2 Diabetes · Insulin resistance · Glucose tolerance · Dietary fbre Introduction composition, named “dysbiosis”, in prediabetic or T2D patients compared to healthy subjects [2, 3]. However, no The gut microbiota is a complex and dynamic ecosystem specifc microbial communities related to the onset of these that interacts with the host while maintaining a mutualistic diseases have been identifed so far. relationship with it. Indeed, it may infuence multiple physi- Nevertheless, more evidence is available on the microbial ological mechanisms related to human health, i.e. synthesis activities linked to the benefcial efect of the gut microbiota of micronutrients, defence against pathogens, regulation of against T2D [4]. The main mechanisms can be summarized glucose and lipid metabolism, and immune function [1]. as follows: (1) maintenance of the integrity of intestinal Therefore, it has been suggested that the modulation of barrier; (2) reduction in bacteria translocation and, conse- gut microbiota could be a reliable tool to prevent metabolic quently, systemic infammation (endotoxemia); (3) produc- and infammatory diseases. In particular, animal studies tion of short-chain fatty acids (SCFA) (acetate, propionate support a causal role between the composition of the gut and butyrate) which can infuence metabolic pathways [5]. microbiota and development of obesity, insulin resistance The frst two efects (maintenance of intestinal barrier and and type 2 diabetes (T2D). In addition, observational stud- reduction in endotoxemia) seem to be more closely linked to ies have confrmed the presence of altered gut microbiota the onset of diseases. Conversely, the production of SCFA could represent a tool to both prevent and modulate T2D [6, 7]. Managed by Massimo Federici . Against this background, several researches have been carried out to identify potential strategies to induce specifc * Angela Albarosa Rivellese [email protected] changes in the gut microbiota composition towards micro- bial species with high fermentative activity. 1 Department of Clinical Medicine and Surgery, University Gut microbiota composition is infuenced by internal and of Naples “Federico II”, 5 Sergio Pansini, 80131 Naples, external factors. Recently, it was shown that genetics plays Italy a marginal role in the defnition of microbiota composi- 2 Task Force On Microbiome Studies, University of Naples tion [8]. As for external factors, faecal transplantations and “Federico II”, Naples, Italy Vol.:(0123456789)1 3 1132 Acta Diabetologica (2021) 58:1131–1138 antibiotics have dramatic but temporary efects on the host microbiota [9]. Conversely, dietary changes could be more efective to induce lasting changes in the composition of gut microbiota. Among dietary components, dietary fbres play a pivotal role. In fact, it is well known that fbres are the main substrate for bacterial metabolism. Furthermore, recent fndings demonstrated that habitual fbre intake can endorse a “virtuous cycle”, consisting in the overgrowth of fbre-fermenting microbial groups while inhibition of other species [10]. Within this context, the prebiotic efect of dietary fbres might be a feasible strategy to prevent T2D, through the modulation of metabolic response. However, to date, there is no conclusive evidence to support this thesis, likely due to the lack of studies focusing primarily on the relationship between the composition of the gut microbiota and meta- Fig. 1 bolic response. Flow diagram of literature search Therefore, in this review, we summarized current evi- dence from observational and intervention studies performed glucose tolerance, prediabetes and T2D. Greater abundance in humans investigating the relationship between the com- of butyrate-producing bacteria was observed in individuals position of the gut microbiota, concentration of SCFA and with normal glucose tolerance than the other two groups. glucose metabolism. Furthermore, the possible mechanisms In line with these results, metagenomic studies showed underlying this association were also discussed. signifcant diferences in the composition of the gut micro- biota of healthy patients compared to diabetic patients in two separate cohorts in China and Europe. In particular, Rose- Methods buria and Faecalibacterium prausnitzii were identifed as highly discriminating bacteria between normoglycaemic Literature searching for this review was conducted by individuals and those with T2D [13, 14]. In addition, in a searching PubMed database for observational studies and cohort of 900 healthy individuals, Senna et al. [15] observed randomized controlled clinical trials on humans adults pub- that the abundance of butyrate-producing bacteria is associ- lished in the English language, during the last 20 years. The ated with a better insulin response during an oral glucose terms “dietary fbre OR fbre OR fbre-rich diet”, “short- tolerance test, i.e. a proxy of improved β cell function. chain fatty acids OR butyrate OR acetate OR propionate”, Looking at how dietary habits may infuence the com- “microbiota OR microbiome OR bacteria”, “type 2 diabetes position of the gut microbiota, the study by De Filippo OR prediabetes OR glucose intolerance OR insulin resist- et al. [16] pointed out relevant diferences in the compo- ance OR insulin response”, combined with the Boolean sition of gut microbiota in children from Africa and Italy. operator “AND”, were employed for the research. Specifcally, African children had increased Bacteroides This review includes studies published in journals in (mainly Prevotella and Xylanibacter) and reduced Firmi- the highest impact factor quartile in the “Endocrinology cutes, whereas Italian children presented an inverse trend. and Metabolism” or “Nutrition and Dietetics” areas. We This fnding can be ascribed to diferent dietary habits in the excluded reviews, acute studies and those not specifcally two cohorts: the former used to a plant-based diet (minor related to each issue of interest. Overall, our search retrieved cereals like millet and sorghum, legumes and vegetables) a total of 18 studies suitable for our review, 10 observational than the latter consuming an animal-based diet rich in fat studies and 8 randomized controlled trials (Fig. 1). and protein. This hypothesis is supported by the presence of bacterial strains that hydrolyse fbres, in particular cellulose and xylans, inducing a greater production of faecal SCFA in Observational studies African children compared to Italian children. As for other dietary pattern, the relationship between Observational studies showed that the composition of the Mediterranean Diet (MD), characterized by a high-fbre gut microbiota is strictly related to the host metabolic state intake, and microbial fermentation was explored in diferent (Table 1). In particular, two large cohort studies [11, 12] studies. Many authors highlighted that the more adhesion to analysed the composition of microbiota into three groups MD, the greater increase of Bacteroides abundance, mainly of individuals with different glucose tolerance: normal Prevotella [17, 18], or Bifdobacteria [19] and Roseburia 1 3 Acta Diabetologica (2021) 58:1131–1138 1133 Table 1 Evidence from observational studies Reference Participants Main results [11] 44 healthy individuals, BMI 23.4 kg/m2 ↑Butyrate-producing bacteria in healthy individuals 64 individuals with pre-diabetes, BMI 24.9 kg/m2 ↑ Bacteroides e costridii in patients with pre-T2D 13 individuals with T2D, BMI 26.5 kg/m2 [12] 206 healthy individuals, BMI 28.2 kg/m2 ↓Butyrate-producing Bacteria both in prediabetes and T2D 220 individuals with pre-diabetes, BMI 28.3 kg/m2 individuals 58 individuals with T2D, BMI 31.6 kg/m2 [13] 53 individuals with T2D, BMI 20–40 kg/m2 ↑Roseburia ↑Faecalibacterium prausnitzii in healthy individuals 49 individuals with pre-diabetes, BMI 20–40 kg/m2 ↓Roseburia ↓Faecalibacterium prausnitzii in individuals with 43 healthy individuals, BMI 20–40 kg/m2 T2D [14] 182 healthy individuals, BMI 18-40Kg/m2 ↑Roseburia ↑Faecalibacterium
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